8Insect Societies as DividedOrganisms: The Complexities ofPurpose and Cross-Purpose

JOAN E. STRASSMANN and DAVID C. QUELLER

Individual organisms are complex in a special way. The organization and function of their parts seem directed toward a purpose: the survival and reproduction of that individual. Groups of organisms are different. They may also be complex, but that is usually because their parts, the individual organisms, are working at cross-purposes. The most obvious exception to this rule is the social insects. Here, the individuals cooperate in complex ways toward the common goal of the success of the colony, even if it means that most of them do not reproduce. Kin selection theory explains how this can evolve. Nonreproductive individuals help in the reproduction of their kin, who share and transmit their genes. Such help is most favored when individuals can give more to their kin than they give up by not reproducing directly. For example, they can remain at their natal site and help defend a valuable resource (“fortress defenders”), or they can ensure that at least one adult survives to care for helpless young (“life insurers”). Although kin selection explains the extensive cooperation and common purpose of social insect colonies, it also predicts a certain amount of cross-purpose and conflict behavior. Kin selection has predicted how workers and queens disagree over sex ratios, how potential queens struggle to be the colony’s head, how workers try to produce sons, and how other workers often prevent them. Kin

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8 Insect Societies as Divided Organisms: The Complexities of Purpose and Cross-Purpose--JOAN E. STRASSMANN and DAVID C. QUELLER ."
In the Light of Evolution: Volume I: Adaptation and Complex Design . Washington, DC: The National Academies Press,
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8
Insect Societies as Divided
Organisms: The Complexities of
Purpose and Cross-Purpose
JoAn e. sTrAssMAnn and DAviD C. QUeller
Individual organisms are complex in a special way. The organiza-
tion and function of their parts seem directed toward a purpose:
the survival and reproduction of that individual. Groups of organ-
isms are different. They may also be complex, but that is usually
because their parts, the individual organisms, are working at
cross-purposes. The most obvious exception to this rule is the
social insects. Here, the individuals cooperate in complex ways
toward the common goal of the success of the colony, even if it
means that most of them do not reproduce. Kin selection theory
explains how this can evolve. Nonreproductive individuals help in
the reproduction of their kin, who share and transmit their genes.
Such help is most favored when individuals can give more to their
kin than they give up by not reproducing directly. For example, they
can remain at their natal site and help defend a valuable resource
(‘‘fortress defenders’’), or they can ensure that at least one adult
survives to care for helpless young (‘‘life insurers’’). Although kin
selection explains the extensive cooperation and common pur-
pose of social insect colonies, it also predicts a certain amount of
cross-purpose and conflict behavior. Kin selection has predicted
how workers and queens disagree over sex ratios, how potential
queens struggle to be the colony’s head, how workers try to
produce sons, and how other workers often prevent them. Kin
Department of ecology and evolutionary Biology, rice University, houston, TX 77005.

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/ Joan E. Strassmann and David C. Queller
selection analysis of cooperation and conflict in social insects is
one of the outstanding achievements of evolutionary theory.
THE ROCK, THE CLOCK, AND ORGANISMAL COMPLEXITY
D
arwin built his theory of descent with modifications from many
quarters. he took uniformitarianism from the geologist Charles
lyell, the struggle for existence from the economist Thomas
Malthus, and homology from a number of continental biologists. Perhaps
most surprising is his debt to a theologian, William Paley. At university,
Darwin had Paley’s Natural Theology (Darwin, 1887b) almost by heart.
Paley pointed to the complexity of organisms and claimed that such com-
plexity required a supernatural intelligence. Darwin’s chief achievement
was to provide a scientific explanation for adaptive complexity.
Paley had famously built his argument from a rock and a clock (Paley,
1802). A stone, he argued, did not beg for any special explanation. it was
simple, predictable, unchanging, devoid of obvious purpose. it might have
been put there by some intelligence, but nothing about it begged for that
explanation. A watch told a different story. The gears, levers, and springs
work together in intricate harmony, causing the hands to move across
the labeled face and measure time. such complexity of design or purpose
could not arise by chance. The watch must have had a designer, a watch-
maker. Paley then applied the argument to organisms and their parts.
The eye has a complex arrangement of parts that have a clear purpose,
endowing its bearer with sight, and such complexity of purpose seemed
to imply a designer and a maker. Throughout the rest of the book, Paley
polishes the argument and applies it to other cases, including the sting of
the worker honey bee, which he called a neutral bee.
Darwin won the argument with Paley long ago. Both had candidate
explanations for complexity, but only Darwin also described a natural
mechanism for adaptation and a natural explanation for the changes
observed in fossils. only Darwin explained aspects of biology that were
nonadaptive consequences of history, from vestigial organs and other
homologies to biogeographical patterns. our understanding that organ-
isms are a mix of historical constraint and adaptation by natural selection
has led to many successful predictions about the natural world, whereas
Paley’s theory stands mute about the details. in other words, Darwin’s
theory is much richer than a simple explanation for design; it makes
many further extensions and predictions. some of these extensions and
predictions were not fully appreciated in Darwin’s time. The last several
decades have seen increased attention to a further important question

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Insect Societies as Divided Organisms /
about the apparent design of organisms. A good theory of design also
ought to explain what kinds of entities are adapted and what kinds of
complexity they show.
organisms, together with man-made machines, seem to show a
unique kind of complexity. We will call this the ‘‘complexity of purpose.’’
‘‘Purpose,’’ as used here, is a metaphor, just as ‘‘natural selection’’ is a
metaphor and has no real selector. This kind of complexity can even be
used to define biological organisms. The organism is the consolidated unit
of design or adaptation; almost everything in the organism seems built
to further the individual’s survival and reproduction (Queller, 1997). Few
parts of the organism are organized to gain at the expense of other parts,
and few parts of the organism are organized to benefit other organisms
(the chief exception being offspring).
The same cannot generally be said about groups of organisms. how
does a flock of birds compare with the rocks and clocks? The parts of a flock
of birds, the individual birds themselves, do not generally appear organized
to benefit the flock. To the contrary, the members compete for food and
mates, sometimes by physical fights, and they hide behind each other as
shields against predation. Groups of organisms, e.g., flocks, populations,
species, and communities, are not themselves clock-like or organismal.
neither are they like the rock, because they are far more complex. But
in contrast to the complexity of purpose shown by organisms, these aggre-
gates have what we call the ‘‘complexity of cross-purpose.’’ The behavior
of flocks, populations, and communities is extraordinarily rich, but not
in a predictable and unified manner like the meshing of gears in a watch.
instead, much of the complexity stems from indifference of the parts to
other parts and the apparent striving of each part to further its own sur-
vival and reproduction, if necessary at the expense of other parts.
evolutionary theory has been addressing this issue of what kinds
of units are adapted, and as it has done so, an interesting puzzle has
emerged. The entities that we recognize as individual organisms actually
originated as groups of lower-level units (Buss, 1987; Maynard smith
and szathmáry, 1995). somehow, the first cell assembled a group of com-
ponents sufficient to sustain replication. The eukaryotic cell began as an
assemblage of several prokaryotic cells, with at least the mitochondria and
chloroplasts having independent origins. larger organisms are groupings
of cells. if groups show cross-purpose, how did they combine and make
the transition to the unity of purpose of a single organism?
social insect groups can give us special insight into this question.
We will argue that social insect colonies are much like organisms, and
we will show how their unity of purpose can arise through kin selec-
tion. We will also show that some cross-purpose remains, that colonies
are not perfectly coherent. These remaining conflicts might be viewed as

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compromising the organismal nature of the colony. But a closer look at
traditional individuals shows that they too have some internal conflicts
(Burt and Trivers, 2006; haig, 1996; hurst et al., 1996). For example, selfish
genetic elements such as transposons can not only make up large parts
of genomes, using expensive resources and extending replication times,
but they can also interfere with the functioning of the individual (Burt
and Trivers, 2006). The conflicts within cooperative social insect colonies
have helped biologists to identify conflict in other cooperative entities, for
example the conflicts between maternal and paternal genes mediated by
genomic imprinting (haig, 2000).
A HOUSE DIVIDED
A small stingless bee out in a tropical forest might seem like any
other animal as it searches for food to survive and reproduce. Upon closer
inspection, a more complex picture would emerge. The foraging bee is a
member of a complex colony inside a tree hollow. Within, there is a citadel
of wax with a smooth protective skin surrounding fat peripheral cells that
contain honey and pollen, and central combs of smaller brood cells, all
held together and supported by a lacy network of wiry wax struts. small
female worker bees are busy everywhere, bringing in food and propolis,
adding to the structures, cleaning, and guarding. But the focus of their
attention is a single female, the queen, with a greatly distended abdomen
and worn, useless wings. A throng of workers surrounds the queen so
closely as to slow her approach to an empty cell. At the empty cell, the
queen antennates the inside, as if checking its construction. The workers
dart in and out, at one time crouching before the queen, at other times
rearing up before her. This agitated ballet ends with the queen stroking
the workers, who then regurgitate larval food into the cell, one after the
other, until it is full. Then the queen lays a single egg that floats on the
provisions. When she leaves, the workers carefully bend the collar of wax
over and close the cell. The egg will hatch and grow to adulthood undis-
turbed but benefiting from the workers’ attention to climate control and
defense (Zucchi, 1993).
This scene summarizes what is special about social insects: complex
communication and integration of behavior, and individuals caring for
the offspring of another. The colony as a whole appears to have the kind
of integration and common purpose normally associated with individual
organisms, with the parts subservient to the whole. The stingless bee
colony is highly organized, both structurally and behaviorally. The pro-
visioning and oviposition process seems to have an almost clock-like
precision, with elaborate coordination between the queen who lays the
egg and the workers who build and provision the cell. This process only

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Insect Societies as Divided Organisms /
works as a whole. if any step in the provisioning and oviposition process
is omitted, the whole operation may fail.
For societies with this level of organization, it is no wonder that the
claim for organismal status of groups has sometimes been made (seeley,
1989; Wheeler, 1911). if this claim stands up to scrutiny, it is extraordinary
in two ways because we think of organisms as consolidated units in two
senses: they are both physically contiguous and genetically uniform.
An organism is typically one solid, connected mass. if it is a single
cell, it is bounded by a membrane; if it is multicellular, the cells abut one
another and form a discrete larger unit. if a social insect colony is an
organism, however, it is a divided one, with parts (the individuals) freely
moving past each other and only occasionally coming into direct contact.
other organisms with separated parts are known. A lizard may detach its
tail to save itself from a predator, and the tail continues to twitch, distract -
ing the predator long after the main body of the lizard has escaped. simi-
larly, when a honey bee worker stings a foe, the barbed sting can easily
detach from the honey bee’s body, and when it does, the sting continues
to dig into the victim’s skin and the poison sac continues to contract and
deliver more of its venom. But these detached organs act independently
for only a brief time before expiring. Moreover, these parts are clearly
secondary, in the sense that a joining of trunk and tail did not form the
lizard. instead, tails are normally attached parts of the organism, both in
the lizard itself and in its relatives with nondetachable tails. A social insect
superorganism, on the other hand, is built from the very beginning of
detached parts. Physical attachment is rare and ephemeral, such as when
army ant workers interlock to form a sheltering bivouac.
A typical organism is also genetically homogeneous. Again, social
insect colonies differ from this standard. in the simplest colony structure,
all members are offspring of a single queen and her mate, so they share
many genes, but each receives its own unique combination of parental
genes. in other species, this genetic distinctness is exacerbated by the pres-
ence of multiple queens or multiple mates. This genetic structure is utterly
different from the clonal, mitotically derived set of cells that constitute a
typical multicellular organism (Maynard smith, 1988). Given that natural
selection operates by favoring genes that pass copies into the next genera -
tion, it is little surprise that a clonal entity can evolve cooperation. if social
insect colonies lack this unity of genotype, what gives them the unity of
purpose that makes them an organism rather than a contentious flock?
HOW ARE COLONIES ORGANISMAL?
it is not hard to view a termite castle, an army ant bivouac, or a wasp
colony as a single, coordinated organism. each shows division of labor,

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with specialization for reproduction, nutrition, communication, defense,
and often thermoregulation. seemingly autonomous individuals are actu-
ally workers whose function appears directed entirely to the whole, such
as a worker who fans the colony to cool it or one who lives her life as a
living honey storage pot (seeley, 1989). The earliest analogies with multi-
cellular organisms focused on these physiological processes and led to
Wilson’s physiologically oriented definition of a superorganism (Wheeler,
1911; Wilson, 1971; hölldobler and Wilson, 1990; Bonner, 2006). But the
analogy could not be pushed too far, perhaps because of fundamental
differences between the physiology of a divided organism (with sepa-
rately mobile individuals) and a multicellular organism. The mobility of
individuals means information and resources can be walked throughout
the colony with no need for specialized structures.
Mobility may therefore underlie the relatively small number of castes
in social insects. Castes are in some ways analogous to cell types in multi -
cellular organisms. each caste or cell type specializes in certain tasks, with
the division of labor aiding the whole. All social insects have functional
reproductive and worker roles, but only some are morphologically dif-
ferentiated into queen and worker castes. A fraction of these species have
multiple worker castes, with the primary distinction being between small
foragers and large soldiers (Wilson, 1971). even highly specialized func-
tions, such as being a honey storage vessel in honeypot ants or using one’s
head to block the colony entrance in Colobopsis ants, are usually performed
by castes that also have more general functions.
Fig. 8.1 shows the complexity, measured as the number of types of sub-
units, of social insect colonies, compared with multicellular individuals.
in one sense, of course, social insect colonies are more complex than
multicellular individuals because the colonies include all of the complex -
ity of their constituent individuals and then add more complexity at the
colony level. But it is still interesting to compare the degree of complexity
added by the specialization of parts in the two cases. Following Bonner
(2006), as a measure of the complexity of specialization, we use cell-type
number and caste number to represent the complexity of individuals and
colonies, respectively. We are unable to use phylogenetically independent
contrasts, but Fig. 8.1 well illustrates how depauperate in specialized
castes social insects are compared with cell specialization in organisms, a
pattern that is unlikely to disappear when analyses are performed with
accurate phylogenies. Complexity increases with the number of units, the
units being cells for organisms and individuals for colonies (Fig. 8.1). The
lower complexity of colonies can be explained partly by size. on average,
social insect colonies do not have as many units as multicellular animals;
colonies rarely have more than a million individuals, whereas large organ-
isms have billions of cells. But that is not the complete explanation. The

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2. 5
log cell types or castes
o cell types
2. 0
+ castes
1. 5
1. 0
0. 5
0. 0
1 2 3 4 5 6 7 8 9 10 11 12 13 14
log cells or individuals
FiGUre 8.1 The number of specialized types (cell types or worker castes) as a
function of the number of units (cells in an organism or number or individuals
in a colony). Cell data (open circles) are from Bell and Mooers (1997). Caste
data (crosses) are for ants and were compiled by Bonner (1993) from data in
hölldobbler and Wilson (1990) and from judgments of caste number by e. o.
Wilson (Bonner, 1993). Mean colony sizes were used when available; when they
were not available, we used the midpoint of the range.
specialization complexity of insect societies is lower for a given number
of units than the complexity of multicellular organisms. This conclusion
seems fairly clear despite the difficulties inherent in defining the number
of castes or cell types, for which we have relied on the judgments of others
(see Fig. 8.1). social insects almost never have even as many as five castes,
whereas many small multicellular organisms attain 10, or many more, cell
types. We suggest that the mobility of the separate parts of a social insect
colony reduces the need for specialized types at the level of the colony.
Despite the limitations of the physiological superorganism model, the
superorganism view can be useful, not only for understanding divided
organisms but also for stimulating new ways to view traditional organisms.
Colonies may not have the same kinds of systems as animals and plants
for fulfilling colony functions, just as in typical organisms the parts of a
colony are subordinate to the whole. As Darwin himself noted, ‘‘. . . if on
the whole the power of stinging be useful to the social community, it will
fulfill all of the requirements of natural selection, although it may cause
the death of some few members’’ (Darwin, 1872, p. 163). A colony can be
viewed as an organism simply because it is highly adapted at the colony
level. of course, this logic does not apply to just any social community, so
the social insects force the question of how some entities become organ -
ismal while others do not.
Although social insect colonies may not have physiologies that closely
match those of multicellular organisms, they do have their own systems for

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defense, nutrition, and reproduction. Close study of any social insect spe-
cies would reveal examples of individual traits that have evolved for colony
function, but the honey bee is the best-studied case. For example, honey
bees use floral food sources, and they need to track this ever-changing
resource. Their famous dance language allows workers to communicate the
quality and location of a resource to nestmate workers. But they also have
mechanisms to effectively allocate work among multiple food sources, even
when each individual has quite limited information. Fidelity to a good
food source is not absolute; a fraction of workers always seeks to discover
new food sources. returning foragers adjust the intensity of their waggle
dancing (the number of waggle runs) according to the profitability of their
trip. Foragers from better sources therefore recruit more followers, so the
colony concentrates on the better food source (seeley, 1997).
Foragers can also tune the intensity of their recruitment dances accord-
ing to how much the colony needs food, but this requires coordination
with the workers that specialize in nectar processing. if a colony needs
more nectar, the nectar-processing bees that have this information crowd
closer to the hive entrance. This means that a returning forager unloads
her nectar quickly, which cues her to intensify her dancing to recruit
more foragers (seeley, 1997) and allay the shortage of nectar. on the other
hand, there may sometimes be more nectar coming into the colony than
the nectar processors can handle, resulting in inefficiently long unloading
times. in this event, foragers perform the tremble dance, which is differ-
ent from the waggle dance in that it stimulates other workers to become
nectar processors (seeley, 1997).
such integrated behaviors of many workers in a honey bee colony
allow the colony to find and exploit food efficiently, to alter group forag-
ing based on individual information, and to adjust the number of foragers
and nectar processors to meet changing needs. no individual is doing
anything that by itself would be very useful; instead, each is performing a
role in a process that only makes sense in terms of increasing colony func -
tion. such a smooth coordination among workers in finding, harvesting,
and processing food makes the argument for the colony as an organism
compelling. similar kinds of coordination are found wherever they are
looked for in social insects, for example, in nest construction in Polybia
wasps (Jeanne, 1986), in nest-finding in honey bees (seeley and visscher,
2004) and Leptothorax ants (Mallon et al., 2001), and in the establishment
of foraging trails by army ants (Franks et al., 1991).
THE SUCCESS OF SOCIAL INSECTS
if colonies have found ways to be more efficient than separate indi -
viduals, one might expect social insects to be particularly successful. in

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fact, they are fantastically successful, particularly the ants and termites,
but also the bees and wasps (Wilson, 1987). success can be measured as
current ecological success, e.g., geographic diversity, species richness, and
biomass. Ants are very speciose and are native to all terrestrial habitats
except Antarctica, iceland, Greenland, and a few remote islands (Wilson,
1987). At one thoroughly studied location in the Amazonian forest, social
wasps, ants, bees, and termites make up four-fifths of all insect biomass
and over a fifth of all animal biomass (Fittkau and Klinge, 1973).
success can also be measured in evolutionary antiquity, staying
power, and diversity. social insects are represented in the fossil record by
impressions of their bodies and their nests. The fossils of bodies are most
useful for tying these insects to extant lineages, whereas the fossil nests
demonstrate clear evidence of ancient sociality. Body fossils of presumably
social termites, ants, bees, and wasps are found in the Cretaceous, whereas
nest fossils are found for some lineages as early as the Triassic (Grimaldi
et al., 1997; hasiotis, 2003; Bordy et al., 2004). only an origin before the
breakup of Pangaea in the late Triassic is consistent with the worldwide
extent of major social insect lineages. The dispersion of major social insect
lineages was essentially complete before the high sea levels of the late
Cretaceous isolated many land masses 100 Mya (hasiotis, 2003; Bordy et
al., 2004). Another indication of the evolutionary robustness of the social
habit is the absence of clear evidence for major lineages of social insects
that subsequently went extinct (Wilson, 1987).
AN INORDINATE FONDNESS FOR KINSHIP
Any theory of adaptation or design ought to explain why social insect
groups are so well adapted while most groups of multicellular organisms
are not adapted. Perhaps the most common feature of insect societies, aside
from their cooperation, is that they are family groups. in some species,
colonies are headed by one singly mated queen (or in termites, a queen
and a king), and all other colony members are full siblings. in others, the
degree of relatedness is lower, but it is nevertheless substantial in all but a
few species of unicolonial insects that are recently derived from those with
higher relatedness. The high relatedness within colonies is often enforced
by overt kin recognition: nonrelatives are recognized and rejected. haldane
once quipped that nature suggests that the creator must have had an inordi-
nate fondness for beetles. With respect to superorganisms, there also seems
to be an inordinate fondness for kinship ties among cooperators.
Darwin had at least an inkling of this: ‘‘As with the varieties of the
stock, so with social insects, selection has been applied to the family, and
not to the individual, for the sake of gaining a serviceable end’’ (Darwin,
1872, p. 230). But the idea was not formalized until W. D. hamilton’s work

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in the 1960s (hamilton, 1964a,b). Taking a gene’s-eye view, hamilton
reasoned that a gene could spread in future generations not only by
contributing to the production of offspring, but also by aiding reproduc-
tion of other relatives who might share the gene. Genetic relatedness
specifies the comparative values of different kin. hamilton’s rule predicts
what behaviors will be favored by selection. A particularly useful form
of hamilton’s rule, for behaviors that exert a fitness cost, c, on some rela-
tives and give a fitness benefit, b, to others, is rbb > rcc. The two fitness
effects are scaled by the relatedness of the actor to those benefited, rb, and
to those harmed, rc. Crucially, individuals can be selected to give up their
own offspring (rc = 1/2) to help other relatives, provided the benefit b is
sufficiently higher than the cost c. Genetic relatedness among individuals
is essential, for without it no value of b, the benefit to cooperation, will
favor giving up reproducing oneself.
THE HAPLODIPLOID HYPOTHESIS
hamilton (1964b) also noticed a special feature of social ants, bees,
and wasps: they share a haplodiploid sex determination mechanism in
which haploid males arise from unfertilized eggs and diploid females
arise from normal fertilized eggs (normark, 2003). This is an ancestral
trait in hymenoptera that arose long before sociality (hamilton, 1967),
but it affects relatednesses in ways that could favor sociality. What makes
it significant for sociality is that sisters are related by 3/4 because they
share all their genes from their haploid father. other things being equal,
a sister would therefore pass on more genes by rearing sisters (r = 3/4)
than by rearing her own progeny (r = 1/2), favoring daughters who
remain with their mothers to rear additional sisters. hamilton noted that
this observation could potentially explain at a stroke at least two salient
feature of social insects (hamilton, 1964b). First, there have been many
origins of sociality in the haplodiploid hymenoptera and few elsewhere,
termites being the most notable exception. second, only females work in
the hymenoptera, whereas both sexes work in diploid termites.
however, this haplodiploid hypothesis is debatable, for a variety
of reasons (Alexander et al., 1991; Queller and strassmann, 1998). First,
most haplodiploids have not evolved sociality, whereas a few diploids
have. Another issue is that relatedness is elevated only to full sisters and
is lowered to brothers (r = 1/4) (Crozier, 1970). Thus, if a female helps to
rear an equal mixture of sisters and brothers, the average relatedness (1/2)
is exactly the same as to her own offspring and exactly the same as full
siblings in diploids. haplodiploidy can still help if workers can concen-
trate on rearing sisters (hamilton, 1972), but the advantage is transitory
and disappears at sex ratio equilibrium (Crozier and Pamilo, 1996).

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Also, the special 3/4 relatedness applies only in colonies with a single,
once-mated queen. Multiple queens and queen replacement reduce related-
ness, as does multiple mating. Accurate estimates of relatedness among
colony members are now available for hundreds of species, typically
based on inherited variation in DnA microsatellite loci (Gadagkar, 1990b;
Crozier and Pamilo, 1996; Peters et al., 1999). Although relatedness among
female colony members in many species is near the full-sister value of 3/4,
in many other species it is lower.
Finally, other possible explanations, some of them noted by hamilton
himself (hamilton, 1964b), have been proposed for the facts the haplo-
diploid hypothesis seems to explain. specifically, the high incidence of
sociality in the hymenoptera and the all-female workforce may relate to
preadaptations involving parental care (Alexander et al., 1991). The soli-
tary hymenoptera have an unusually high level of parental care, meaning
that adaptations for nest-building, prey capture, brood care, sanitation,
and defense are already in place. it must be much easier to evolve allo-
parental care in groups that already have parental care. And because it is
females that provide the parental care in solitary hymenoptera, with spe-
cial adaptations such as the sting, it is not surprising that females provide
the care in social hymenoptera (Alexander et al., 1991).
KIN SELECTION AND SYNERGISM:
LIFE INSURANCE AND FORTRESS DEFENSE
Kin selection has been so closely identified with the haplodiploid
hypothesis that concerns with the latter have caused some to question kin
selection in general. But of course hamilton’s rule does not require that
relatedness to beneficiaries must be higher than relatedness to one’s own
offspring. if rb = rc, or even if rb < rc, hamilton’s rule can still favor altruism
if the benefit is sufficiently greater than the cost (b > c) (West-eberhard,
1975). The question then concerns how it is possible to rear more young
by aiding the beneficiary than by reproducing independently. synergies
from division of labor between helpers and reproducers are easy to see
after sociality has evolved, but this kind of specialization seems unlikely
to be present at the beginning of sociality.
Two kinds of factors seem especially likely to provide the necessary
advantage to helping: ‘‘fortress defense’’ and ‘‘life insurance’’ (Queller
and strassmann, 1998). Fortress defenders live in protected, expandable
sites that generally include food (Andersson, 1984; Alexander et al., 1991;
Crespi, 1994), such as the wood galleries of termites and the plant galls of
social aphids and thrips. An offspring can gain by remaining at the natal
site, even if she has to rear less-related collateral relatives, because she
avoids risking death by migrating to a new site (see Fig. 8.2a). Because

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/ Joan E. Strassmann and David C. Queller
FiGUre 8.2 Fitness advantages of sociality when siblings and offspring are
equally valuable. Arrows show transitions from one time period to another, and
enclosure within dashed rectangles indicates the same nest. (a) leaving vs. For-
tress Defense. if an individual (self) leaves her natal site, she survives dispersal
with probability sd, whereas her mother survives in the safe natal site. Both then
produce offspring. Alternatively, if self stays in the safe site with her mother, she
avoids a bout of dispersal mortality and doubles her mother’s output. (b) leaving
vs. life insurance. here we assume that dispersal carries no cost but that a par-
ent survives the period of parental care with probability sc. if she dies during this
period, her offspring also die. When self stays with her mother, there are three
ways for the offspring to survive: if both adults survive, if only the mother sur-
vives, and if only self survives.

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food is available at the home site, little feeding care is needed, and the first
worker specialists are generally soldiers specialized for defense.
By contrast, life insurers cooperate to ensure that dependent young
survive (Queller, 1989, 1994, 1996; strassmann and Queller, 1989; Gadagkar,
1990a). They can live in a variety of sites, safe or unsafe, but generally have
helpless young that need food and protection. The problem is that an adult
must undertake dangerous foraging for her young, but if she dies during
one of these trips, her still-dependent young also die. But when a daughter
stays at the natal nest to help, and either the mother or the daughter dies,
the survivor can take over feeding and protecting the young, giving rise
to the synergistic advantage (Fig. 8.2b). Wasps, bees, and ants appear to fit
this mold. The crucial assumption that dead individual’s investments can
be saved by its surviving colony mates has been experimentally confirmed
in a stenogastrine wasp (Field et al., 2000). other advantages besides for-
tress defense and life insurance are also possible, and much work remains
to be done on assessing their relative importance.
RELATEDNESS IS STILL IMPORTANT
Whatever the fitness advantages of altruism might be, they are selec-
tively irrelevant unless they go to relatives. hamilton’s kin selection theory
(hamilton, 1964a,b) still provides the framework for understanding altru -
ism, even if the altruism is not driven by extra-high relatedness. As noted
above, the fact that social insect colonies consist of families, and that they
exclude outsiders, shows that relatedness matters. But other studies have
tested more specific predictions about the importance of relatedness.
A recent comparative study of wasps and bees (Wenseleers and
ratnieks, 2006) showed how workers modulate their altruism and selfish -
ness according to relatedness in queenless colonies. Colonies with queens
removed were used because (as we will see below) worker selfishness can
be repressed in colonies with the queen present, either by the queen herself
or by other workers. With the queen gone, some workers develop ovaries
and lay unfertilized eggs that will develop into males. if all workers ceased
working and took up laying eggs, the colony’s production of males would
presumably fall, because a certain number of workers are needed to feed
the larvae. in fact, the queenless colonies never had more than 40% repro-
ductive workers; at least 60% remained as helpers. Most interesting was
the finding that fewer workers laid eggs from species in which relatedness
among workers was high. in other words, more workers stayed in the
altruistic helping mode when relatedness was high. relatedness explained
62% of the variance in percentage of helpers (Wenseleers and ratnieks,
2006). variation in relatedness also predicts variation in helping behavior
in birds and mammals (Griffin and West, 2003).

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Unexpected and powerful evidence of the importance of relatedness
has come from sex ratio studies. As noted above, haplodiploid female
workers are related to full sisters by 3/4 and to brothers by 1/4. This
implies that, other things being equal, these workers ought to prefer
helping sisters (hamilton, 1972). specifically, Trivers and hare (1976)
showed that in a colony with a single once-mated queen, workers should
prefer to invest three times as much in future queens as in males. They
also showed that, in species of ants likely to have a single, once-mated
queen, investment ratios are in fact closer to this 3:1 ratio than to the usual
Fisherian 1:1.
More impressive evidence comes from species with variable related-
ness. When a queen mates multiple times, workers will not favor this 3:1
ratio because the workers are equally related (by 1/4) to half sisters and
brothers (because brothers do not have fathers, multiple mating by the
queen does not change their relatedness). This means that these workers
should rear more males than those in singly mated colonies, and the
frequency-dependent nature of sex ratio selection should cause the two
kinds of colonies to increasingly specialize (Boomsma and Grafen, 1990,
1991). Workers in colonies with singly mated queens should specialize
largely in rearing queens, and workers in colonies with multiply mated
queens should specialize in rearing males. This odd prediction of what
has come to be called ‘‘split sex ratio theory’’ was strikingly confirmed in a
study of the ant Formica exsecta (sundström et al., 1996) and has been con-
firmed in many other species (Queller and strassmann, 1998; Chapuisat
and Keller, 1999; Bourke, 2005).
Besides showing that workers are indeed sensitive to relatedness,
the sex ratio studies made an even more important point: There can be
conflict within these apparently superorganismal colonies. Queens are
equally related to their sons and daughters, so they should prefer the
standard 1:1 sex investment ratio (Trivers and hare, 1976). The resulting
conflict can lead to inefficiencies that are decidedly against the interests of
the superorganism as a whole. For example, the split sex ratio described
above for Formica exsecta is achieved only after some waste. Queens in both
singly and multiply mated colonies laid the same sex ratio of eggs, but
workers in the singly mated colonies achieved their preferred investment
in full sisters by killing many of the male larvae (sundström et al., 1996;
Chapuisat et al., 1997).
it seems paradoxical that this elegant evidence for kin selection theory
comes from conflict rather than from cooperation, but there is really no
contradiction. Kin selection theory shows how individuals can further
the reproduction of their own genes, and this is sometimes achieved by
cooperation and sometimes by conflict.

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AN EVEN MORE INORDINATE FONDNESS FOR SELF
Conflict over sex ratios was an exciting finding, both because of the
support that it provided for kin selection theory and because it showed
that even sterile workers could find ways to pursue interests that were
different from the queen’s. it thus poked a hole in the view of a colony as
superorganismal, a small hole by itself, but one that opened up a vista of
other realms of possible conflict. hamilton’s rule predicts more extensive
conflict over the question of who gets to reproduce. Although typically
related, individuals are genetically separate, and each individual is usually
more related to its own young than to those of a relative. if other things
are equal, hamilton’s rule predicts that each individual would prefer to
take the reproductive role. Thus, even though advantages like fortress
defense or life insurance select for helping instead of going it alone, the
issue of helping is not completely resolved because it is often better, still,
to be helped.
Conflict over reproduction has long been apparent to researchers
working on simple social insect societies that are made up of morpho-
logically identical females, such as Polistes wasps. Colonies are initiated
by single females or by groups of females, who are often sisters. They do
not share reproduction equally. instead, they form dominance hierarchies
(Pardi, 1942; West-eberhard, 1969; strassmann, 1981) enforced by time-
consuming aggression so intense it can result in death, although some spe-
cies have conventions that reduce the battling (hughes and strassmann,
1988; seppä et al., 2002). once the hierarchy is set, the losers function as
workers, if they choose to remain at the nest. But they still may not work
optimally, instead waiting for a chance to reproduce. in Liostenogaster fla-
volineata, a Malaysian stenogastrine wasp that lacks morphological castes,
a queue based on order of arrival determines who succeeds the dominant
queen. When females reach the number two spot in the queue, they work
less hard (Field et al., 2006). in other words, when the option of reproduc-
ing directly appears more likely, they decline to take as many risks on
behalf of their relatives.
The success of predictions of sex ratio conflict led researchers to ask
how much conflict over reproduction remains in highly eusocial insects,
those with morphologically distinct queen and worker castes. Are these
colonies subject to the complexities of cross-purpose?
it turns out that even the most advanced societies are not immune to
this kind of conflict. When it comes time for honey bee colonies to divide,
several half-sister queens are reared with special food in extra-large cells.
The old queen leaves with much of the workforce to start a new colony.
Then, the first of the new queens to emerge as an adult seeks out all of the
other queen cells and uses her sting to kill her sister rivals (Gilley, 2001).

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Why honey bees produce these extra queens is not fully clear, perhaps
as insurance against one of them dying. But they do limit the conflict to a
few individuals by controlling queen production through the special feed-
ing they require. This limitation is extremely common in social insects with
queen and worker castes. Queens generally require more food, offering
the opportunity to control queen production (Wilson, 1971). it is instruc-
tive to see what happens in the unusual cases in which this constraint
does not hold.
in one genus of stingless bees, Melipona, caste is not determined by dif-
ferential feeding. instead, workers and queens develop in cells of the same
size, provisioned with the same amounts of food. This presumably leaves
the choice of being queen up to each developing female larva. As a con-
sequence, a significant fraction of females (5–20%) develop into queens,
with small heads, large abdomens, and lacking the pollen baskets required
to be effective workers (Wenseleers and ratnieks, 2004). Because stingless
bees reproduce by colony division, this amount of queen production is
far more than the single queen they need, every once in awhile, to head a
new colony. The excess queens, useless for work and a potential threat to
the old queen, are slaughtered by workers (Wenseleers et al., 2004). The
5–20% reduction in worker production must constitute a significant cost
to the colony and clearly shows that cross-purpose can remain important
in advanced social insects.
stingless bees other than Melipona determine caste by the usual means
of feeding some larvae more, but this does not entirely solve the problem.
in some species, in which brood cells are adjacent, a larvae that is sup-
posed to be a worker can tunnel from its own cell into its neighbor’s,
consume the food stores intended for its neighbor, and develop as a queen
(engels and imperatriz-Fonseca, 1990). in other species, some individuals
with worker-sized food allotments will nevertheless develop into morpho-
logical queens (Wenseleers et al., 2005). in Schwarziana quadripunctata, these
dwarf queens make up only 0.6% of all individuals reared in worker-sized
cells but 86% of all queens reared. These queens are less successful than
normal-sized queens in attaining reproductive status and are executed
more readily by the workers. still, the strategy appears to be successful
often enough to pay, inasmuch as 22% of all reproductive females are
dwarf queens (Wenseleers et al., 2005). some ant genera, such as Myrmica
and Solenopsis, also have some small queens (called microgynes), which
may be the result of individual larvae determining their own caste fate in
colonies that are initiated by budding (Bourke and Franks, 1995; Mcinnes
and Tschinkel, 1995).
The threat of other queens may lie behind another colony-level design
flaw that is usually not obvious but is present in many species: the lack of
a backup queen. Consider the fungus-growing ants of the genus Atta. A

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mature Atta colony is a huge and intricate operation. Millions of ants culti-
vate fungi deep underground. The nest has chambers a person could stand
in, gardens tended by a suite of worker castes, including leaf processors
who use microbial fungicides and have specialized organs to carry these
symbionts (Currie et al., 2006). however, this metropolis of ants has but a
single queen, and when she dies the colony dies: the fungus gardens are
overrun by rogue fungi, the workers cease to rear brood, and the galleries
ultimately collapse. This disaster could be avoided by the relatively simple
matter of keeping on hand one or more backup queens. But this would risk
unleashing competition among the queens that might harm the interests
of both the current queen and her workers.
WORKER REPRODUCTION AND POLICING
The existence of dwarf queens shows that even larvae that are fed less
than the normal queen amount can reproduce. This ability can also extend
to workers. Workers are females that are morphologically or behavior-
ally specialized to forage, care for brood, and defend the colony. none
of these tasks is enhanced by egg-laying, and yet workers in nearly all
species maintain some ability to lay eggs. Workers in many species regu -
larly do so, producing males because they are uninseminated. They have
considerable incentive to do this because a worker is more related to her
own sons (1/2) than to brothers (1/4) produced by her mother (Trivers
and hare, 1976).
in some species, the queen ‘‘polices’’ these worker-laid male eggs,
eating them when she finds them. indeed the elaborate provisioning and
oviposition process of stingless bees described earlier may sometimes
be less a matter of cooperative communication about the filling of the
cell than a contest over who gets to fill it. All that actually needs to be
accomplished is regurgitation of food into the cell by workers, laying
of an egg by the queen, and then sealing of the cell by workers. As it is,
many more workers than necessary surround the empty cell. When the
queen approaches the empty cell she can be very aggressive toward the
workers, who ritually either approach her or back away. The queen often
aggressively solicits food from the workers, who nearly always refuse to
provide it. After the cell is filled, the queen lays an egg in it. interestingly,
the workers close the cell with their abdomen in it, a position in which they
might lay an egg, something that might account for the commonness of
worker male production in stingless bees (Tóth et al., 2002b). [in some spe-
cies, workers return later to sealed cells to open them and oviposit (Beig,
1972; Tóth et al., 2002a), which can succeed because the worker-laid male
egg hatches quickly, and the larva hunts down and kills the older female
larva in the cell.] The fact that these behavior patterns differ considerably

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between species is consistent with an ‘‘arms race’’ caused by conflict (Why
would a good, efficient communication system need to change rapidly?).
in other words, the complexity of the provisioning process may not be
purposeful clockwork, but more like a boxing match full of punches and
counterpunches. The winner varies from species to species, with queens
producing all of the males in some and workers producing most in others
(Tóth et al., 2004).
if we do not see these elaborate direct contests in other species, it may
be because the stingless bees are rather unusual in mass-provisioning their
brood cells with all of the food before oviposition. This focuses the laying
process on one cell at a time and brings the contenders together. And of
course, workers are favored to produce the males because colonies are
headed by single-once mated queens (Peters et al., 1999).
in other social insects, workers have wider opportunities to lay eggs
when the queen is absent. Policing by the queen then seems unlikely
to succeed in colonies with thousands of workers, so one might expect
workers to take advantage of this lack of control and produce many
males. in some species they do, but in other species, like the honey bee,
the queen still produces all of the males. here, policing of worker-laid
eggs is performed by other workers, in a seeming lapse of class solidarity.
each worker should prefer to lay her own male eggs, but how should she
view the contest between other workers and the queen? When the queen
is mated multiply, as in honey bees, and workers are usually half-sisters,
each worker will prefer the queen’s males (r = 1/4) to those of other
workers (r = 1/8) (ratnieks, 1988). Again we have the inefficiencies of
conflict, with some colony members negating what the others have done.
Workers may be neuter but, to recall Paley’s adjective, they are anything
but neutral. They would prefer to reproduce, but they also prefer not to
let each other reproduce, and therefore they ensure that the queen wins.
oddly, the stronger the policing, the less actual conflict there may be. in
species in which most worker-laid eggs are removed, few workers develop
ovaries and lay eggs (Wenseleers and ratnieks, 2006).
Workers can sometimes win the battle with queens in the most extreme
way possible: by killing the queen (Bourke, 1994). Usually this is not a
beneficial option, because the workers need the queen to produce both
more workers and more reproductive females. But certain social insects
have an annual colony cycle with males produced at the end, which
makes the queen dispensable at the end of the season. Killing her allows
workers to produce all of the males. Again, the choice appears to be
affected by relatedness in ways predicted by kin selection theory: queens
disappear more in singly mated species because those are the species in
which workers favor production of males by other workers (Foster and
ratnieks, 2001).

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CONCLUSIONS
living things are complex, but this complexity is of two broad types.
organisms show complexity of apparent purpose, with all of the parts
acting for the whole. Groups, however, are usually dominated by the
complexities of cross-purpose; the parts seem goal-directed, but the goals
are not shared, and the result is often anything but elegant. The most spec-
tacular exceptions, at the group level, are social insect societies, in which
the individuals usually do seem to act toward a common goal.
Any scientific theory purporting to account for biological complexity
ought to account for this special nature of social insects. Why do their
colonies show a degree of apparent purpose lacking in other aggregations,
herds, and flocks? The kin selection extension of natural selection theory
does explain this; cooperation results from the opportunity to give suf -
ficiently large benefits to kin.
More importantly, kin selection theory has successfully predicted new
findings. Although social insect colonies have clock-like design in many
respects, kin selection theory predicts who is throwing sand into the clock -
works, as well as which gears might be slipped and which springs sprung.
Many of the predicted findings, such as sex ratio conflict and policing,
were otherwise completely unexpected. The success of this approach
shows that the Darwinian paradigm is capable of explaining not just the
adaptations of organisms but also how new kinds of organismal entities
come into being.
ACKNOWLEDGMENTS
We thank F. Ayala and J. Avise for organizing the symposium in
which this work was presented, John Bonner for kindly providing original
data for the social insect portion of Fig. 8.1, and J. J. Boomsma and the
anonymous referees for helpful suggestions. This material is based on
work supported by national science Foundation Grant eF0626963.